Vascular and epithelial junctions: A barrier for leucocyte migration

Biochemical Society Transactions

Volumn 36, Issue 2, 2008, Pages 203-211

  Garrido Urbani, Sarah ^a   Bradfield, Paul F ^a   Lee, Boris P L ^a   Imhof, Beat A ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Adhesion; Immune response; Inflammation; Junctional adhesion molecule (JAM); Leucocyte; Transmigration

Indexed keywords

CD31 ANTIGEN; CD99 ANTIGEN; JUNCTIONAL ADHESION MOLECULE A; TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL CADHERIN;

CONFERENCE PAPER; ENDOTHELIUM CELL; EPITHELIUM CELL; HUMAN; IMMUNE SYSTEM; IMMUNOREACTIVITY; LEUKOCYTE MIGRATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; ENDOTHELIAL CELLS; EPITHELIAL CELLS; HUMANS; INTERCELLULAR JUNCTIONS; LEUKOCYTES; MODELS, IMMUNOLOGICAL;

EID: 42449100831     PISSN: 03005127     EISSN: None     Source Type: Journal    
DOI: 10.1042/BST0360203     Document Type: Conference Paper

References (72)

1. Springer, T.A. (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301-314
2. Feng, D., Nagy, J.A., Pyne, K., Dvorak, H.F. and Dvorak, A.M. (1998) Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med. 187, 903-915
3. Vestweber, D. (2007) Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol. Rev. 218, 178-196
4. Hixenbaugh, E.A., Goeckeler, Z.M., Papaiya, N.N., Wysolmerski, R.B., Silverstein, S.C. and Huang, A.J. (1997) Stimulated neutrophils induce myosin light chain phosphorylation and isometric tension in endothelial cells. Am. J. Physiol. 273, H981-H988
5. i signaling during transmigration of polymorphonuclear leukocytes. Blood 96, 3816-3822
6. Gautam, N., Olofsson, A.M., Herwald, H., Iversen, L.F., Lundgren-Akerlund, E., Hedgvist, P., Arfors, K.E., Flodgaard, H. and Lindbom, L. (2001) Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nat. Med. 7, 1123-1127
7. Marchesi, V.T. and Gowans, J.L. (1964) The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc. R Soc. London Ser. B 159, 283-290
8. Yang, L., Froio, R.M., Sciuto, T.E., Dvorak, A.M., Alon, R. and Luscinskas, F.W. (2005) ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-α-activated vascular endothelium under flow. Blood 106, 584-592
9. Carman, C.V., Sage, P.T., Sciuto, T.E., de la Fuente, M.A., Geha, R.S., Ochs, H.D., Dvorak, H.F., Dvorak, A.M. and Springer, T.A. (2007) Transcellular diapedesis is initiated by invasive podosomes. Immunity 26, 784-797
10. Carman, C.V. and Springer, T.A. (2004) A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J. Cell Biol. 167, 377-388
11. Nieminen, M., Henttinen, T., Mermen, M., Marttila-Ichihara, F., Eriksson, J.E. andjalkanen, S. (2006) Vimentin function in lymphocyte adhesion and transcellular migration. Nat, Cell Biol. 8, 156-162
12. Millan, J., Hewlett, L., Glyn, M., Toomre, D., Clark, P. and Ridley, A.J. (2006) Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat. Cell Biol. 8, 113-123
13. Bird, I.N., Spragg, J.H., Ager, A. and Matthews, N. (1993) Studies of lymphocyte transendothelial migration: analysis of migrated cell phenotypes with regard to CD31 (PECAM-1), CD45RA and CD45RO. Immunology 80, 553-560
14. Engelhardt, B. and Wolburg, H. (2004) Transendothelial migration of leukocytes: through the front door or around the side of the house? Eur. J. Immunol. 34, 2955-2963
15. Huang, A.J., Furie, M.B., Nicholson, S.C., Fischbarg, J., Liebovitch, L.S. and Silverstein, S.C. (1988) Effects of human neutrophil chemotaxis across human endothelial cell monolayers on the permeability of these monolayers to ions and macromolecules. J. Cell. Physiol. 135, 355-366
16. Muller, W.A., Ratti, C.M., McDonnell, S.L. and Cohn, Z.A. (1989) A human endothelial cell-restricted, externally disposed plasmalemmal protein enriched in intercellular junctions. J. Exp. Med. 170, 399-414
17. Bogen, S., Pak, J., Gahfallou, M., Deng, X. and Muller, W.A. (1994) Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J. Exp. Med. 179, 1059-1064
18. Liao, F., Huynh, H.K., Eiroa, A., Greene, T., Polizzi, E. and Muller, W.A. (1995) Migration of monocytes across endothelium and passage through extracellular matrix involve separate molecular domains of PECAM-1. J. Exp. Med. 182, 1337-1343
19. Liao, F., Ali, J., Greene, T. and Muller, W.A. (1997) Soluble domain 1 of platelet-endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo. J. Exp. Med. 185, 1349-1357
20. Nakada, M.T., Amin, K., Christofidou-Solomidou, M., O'Brien, C.D., Sun, J., Gurubhagavatula, I., Heavner, G.A., Taylor, A.H., Paddock, C., Sun, Q.H. et al. (2000) Antibodies against the first Ig-like domain of human platelet endothelial cell adhesion molecule-1 (PECAM-1) that inhibit PECAM-1-dependent homophilic adhesion block in vivo neutrophil recruitment. J. Immunol. 164, 452-462
21. Wakelin, M.W., Sanz, M.J., Dewar, A., Albelda, S.M., Larkin, S.W., Boughton-Smith, N., Williams, T.J. and Nourshargh, S. (1996) An anti-platelet-endothelial cell adhesion molecule-1 antibody inhibits leukocyte extravasation from mesenteric microvessels in vivo by blocking the passage through the basement membrane. J. Exp. Med. 184, 229-239
22. Woodfin, A., Voisin, M.B. and Nourshargh, S. (2007) PECAM-1: a multi-functional molecule in inflammation and vascular biology. Arterioscler. Thromb. Vasc. Biol. 27, 2514-2523
23. Huang, M.T., Larbi, K.Y., Scheiermann, C., Woodfin, A., Gerwin, N., Haskard, D.O. and Nourshargh, S. (2006) ICAM-2 mediates neutrophil transmigration in vivo: evidence for stimulus specificity and a role in PECAM-1-independent transmigration. Blood 107, 4721-4727
24. Wingett, D., Forcier, K. and Nielson, C.P. (1999) A role for CD99 in T cell activation. Cell. Immunol. 193, 17-23
25. Schenkel, A.R., Mamdouh, Z., Chen, X., Liebman, R.M. and Muller, W.A. (2002) CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat. Immunol. 3, 143-150
26. Bixel, G., Kloep, S., Butz, S., Petri, B., Engelhardt, B. and Vestweber, D. (2004) Mouse CD99 participates in T-cell recruitment into inflamed skin. Blood 104, 3205-3213
27. Lampugnani, M.G., Resnati, M., Raiteri, M., Pigott, R., Pisacane, A., Houen, G., Ruco, L.P. and Dejana, E. (1992) A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118, 1511-1522
28. Shaw, S.K., Bamba, P.S., Perkins, B.N. and Luscinskas, F.W. (2001) Real-time imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J. Immunol. 167, 2323-2330
29. Gotsch, U., Borges, E., Bosse, R., Boggemeyer, E., Simon, M., Mossmann, H. and Vestweber, D. (1997) VE-cadherin antibody accelerates neutrophil recruitment in vivo. J. Cell Sci. 110, 583-588
30. Allingham, M.J., van Buul, J.D. and Burridge, K. (2007) ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J. Immunol. 179, 4053-4064
31. Bazzoni, G. (2003) The JAM family of junctional adhesion molecules. Curr. Opin. Cell Biol. 15, 525-530
32. Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A. et al. (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142, 117-127
33. Del Maschio, A., De Luigi, A., Martin-Padura, I., Brockhaus, M., Bartfai, T., Fruscella, P., Adorini, L., Martino, G., Furlan, R., De Simoni, M.G. and Dejana, E. (1999) Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J. Exp. Med. 190, 1351-1356
34. Johnson-Leger, C.A., Aurrand-Lions, M., Beltraminelli, N., Fasel, N. and Imhof, B.A. (2002) Junctional adhesion molecule-2 (JAM-2) promotes lymphocyte transendothelial migration. Blood 100, 2479-2486
35. Bradfield, P.F., Nourshargh, S., Aurrand-Lions, M. and Imhof, B.A. (2007) JAM family and related proteins in leukocyte migration (Vestweber series). Arterioscler. Thromb. Vasc. Biol. 27, 2104-2112
36. Lechner, F., Sahrbacher, U., Suter, T., Frei, K., Brockhaus, M., Koedel, U. and Fontana, A. (2000) Antibodies to the junctional adhesion molecule cause disruption of endothelial cells and do not prevent leukocyte influx into the meninges after viral or bacterial infection. J. Infect. Dis. 182, 978-982
37. Liu, Y., Nusrat, A., Schnell, F.J., Reaves, T.A., Walsh, S., Pochet, M. and Parkos, C.A. (2000) Human junction adhesion molecule regulates tight junction resealing in epithelia. J. Cell Sci. 113, 2363-2374
38. Ostermann, G., Weber, K.S., Zernecke, A., Schroder, A. and Weber, C. (2002) JAM-1 is a ligand of the β2 integrin LFA-1 involved in transendothelial migration of leukocytes. Nat. Immunol. 3, 151-158
39. Ozaki, H., Ishii, K., Horiuchi, H., Arai, H., Kawamoto, T., Okawa, K., Iwamatsu, A. and Kita, T. (1999) Cutting edge: combined treatment of TNF-α and IFN-γ causes redistribution of junctional adhesion molecule in human endothelial cells. J. Immunol. 163, 553-557
40. Cera, M.R., Del Prete, A., Vecchi, A., Corada, M., Martin-Padura, I., Motoike, T., Tonetti, P., Bazzoni, G., Vermi, W., Gentili, F. et al. (2004) Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J. Clin. Invest. 114, 729-738
41. Matsutani, T., Tanaka, T., Tohya, K., Otani, K., Jang, M.H., Umemoto, E., Taniguchi, K., Hayasaka, H., Ueda, K. and Miyasaka, M. (2007) Plasmacytoid dendritic cells employ multiple cell adhesion molecules sequentially to interact with high endothelial venule cells: molecular basis of their trafficking to lymph nodes. Int. Immunol. 19, 1031-1037
42. Corada, M., Chimenti, S., Cera, M.R., Vinci, M., Salio, M., Fiordaliso, F., De Angelis, N., Villa, A., Bossi, M., Staszewsky, L.I. et al. (2005) Junctional adhesion molecule-A-deficient polymorphonuclear cells show reduced diapedesis in peritonitis and heart ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U.S.A. 102, 10634-10639
43. Woodfin, A., Reichet C.A., Khandoga, A., Corada, M., Voisin, M.B., Scheuermann, C., Haskard, D.O., Dejana, E., Krombach, F. and Nourshargh, S. (2007) JAM-A mediates neutrophil transmigration in a stimulus-specific manner in vivo: evidence for sequential roles for JAM-A and PECAM-1 in neutrophil transmigration. Blood 110, 1848-1856
44. Palmeri, D., van Zante, A., Huang, C.C., Hemmerich, S. and Rosen, S.D. (2000) Vascular endothelial junction-associated molecule, a novel member of the immunoglobulin superfamily, is localized to intercellular boundaries of endothelial cells. J. Biol. Chem. 275, 19139-19145
45. Arrate, M.P., Rodriguez, J.M., Tran, T.M., Brock, T.A. and Cunningham, S.A. (2001) Cloning of human junctional adhesion molecule 3 (JAM3) and its identification as the JAM2 counter-receptor. J. Biol. Chem. 276, 45826-45832
46. Cunningham, S.A., Arrate, M.P., Rodriguez, J.M., Bjercke, R.J., Vanderslice, P., Morris, A.P. and Brock, T.A. (2000) A novel protein with homology to the junctional adhesion molecule: characterization of leukocyte interactions. J. Biol. Chem. 275, 34750-34756
47. Cunningham, S.A., Rodriguez, J.M., Arrate, M.P., Tran, T.M. and Brock, T.A. (2002) JAM2 interacts with α4β1: facilitation by JAM3. J. Biol. Chem. 277, 27589-27592
48. Ludwig, R.J., Zollner, T.M., Santoso, S., Hardt, K., Gille, J., Baatz, H., Johann, P.S., Pfeffer, J., Radeke, H.H., Schon, M.P. et al. (2005) Junctional adhesion molecules (JAM)-B and -C contribute to leukocyte extravasation to the skin and mediate cutaneous inflammation. J. Invest. Dermatol. 125, 969-976
49. Bradfield, P.F., Scheiermann, C., Nourshargh, S., Ody, C., Luscinskas, F.W., Rainger, G.E., Nash, G.B., Miljkovic-Licina, M., Aurrand-Lions, M. and Imhof, B.A. (2007) JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood 110, 2545-2555
50. Santoso, S., Sachs, U.J., Kroll, H., Linder, M., Ruf, A., Preissner, K.T. and Chavakis, T. (2002) The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J. Exp. Med. 196, 679-691
51. Chavakis, T., Keiper, T., Matz-Westphal, R., Hersemeyer, K., Sachs, U.J., Nawroth, P.P., Preissner, K.T. and Santoso, S. (2004) The junctional adhesion molecule-C promotes neutrophil transendothelial migration in vitro and in vivo. J. Biol. Chem. 279, 55602-55608
52. Aurrand-Lions, M., Lamagna, C., Dangerfield, J.P., Wang, S., Herrera, P., Nourshargh, S. and Imhof, B.A. (2005) Junctional adhesion molecule-C regulates the early influx of leukocytes into tissues during inflammation. J. Immunol. 174, 6406-6415
53. Randolph, G.J. and Furie, M.B. (1996) Mononuclear phagocytes egress from an in vitro model of the vascular wall by migrating across endothelium in the basal to apical direction: role of intercellular adhesion molecule 1 and the CD11/CD18 integrins. J. Exp. Med. 183, 451-462
54. Hirabayashi, S., Tajima, M., Yao, I., Nishimura, W., Mori, H. and Hata, Y. (2003) JAM4, a junctional cell adhesion molecule interacting with a tight junction protein, MAGM. Mol. Cell. Biol. 23, 4267-4282
55. Wegmann, F., Ebnet, K., Du Pasquier, L., Vestweber, D. and Butz, S. (2004) Endothelial adhesion molecule ESAM binds directly to the multidomain adaptor MAGI-1 and recruits it to cell contacts. Exp. Cell Res. 300, 121-133
56. Nasdala, I., Wolburg-Buchholz, K., Wolburg, H., Kuhn, A., Ebnet, K., Brachtendorf, G., Samulowitz, U., Kuster, B., Engelhardt, B., Vestweber, D. and Butz, S. (2002) A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J. Biol. Chem. 277, 16294-16303
57. Wegmann, F., Petri, B., Khandoga, A.G., Moser, C., Khandoga, A., Volkery, S., Li, H., Nasdala, I., Brandau, O., Fassler, R. et al. (2006) ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med. 203, 1671-1677
58. Zen, K., Liu, Y., McCall, I.C., Wu, T., Lee, W., Babbin, B.A., Nusrat, A. and Parkos, C.A. (2005) Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol. Biol. Cell 16, 2694-2703
59. Mirza, M., Hreinsson, J., Strand, M.L., Hovatta, O., Soder, O., Philipson, L., Pettersson, R.F. and Sollerbrant, K. (2006) Coxsackievirus and adenovirus receptor (CAR) is expressed in male germ cells and forms a complex with the differentiation factor JAM-C in mouse testis. Exp. Cell Res. 312, 817-830
60. Gliki, G., Ebnet, K., Aurrand-Lions, M., Imhof, B.A. and Adams, R.H. (2004) Spermatid differentiation requires the assembly of a cell polarity complex downstream of junctional adhesion molecule-C. Nature 431, 320-324
61. Nagamatsu, G., Ohmura, M., Mizukami, T., Hamaguchi, I., Hirabayashi, S., Yoshida, S., Hata, Y., Suda, T. and Ohbo, K. (2006) A CTX family cell adhesion molecule, JAM4, is expressed in stem cell and progenitor cell populations of both male germ cell and hematopoietic cell lineages. Mol. Cell. Biol. 26, 8498-8506
62. Parkos, C.A., Delp, C., Arnaout, M.A. and Madara, J.L. (1991) Neutrophil migration across a cultured intestinal epithelium: dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J. Clin. Invest. 88, 1605-1612
63. Parkos, C.A., Colgan, S.P., Diamond, M.S., Nusrat, A., Liang, T.W., Springer, T.A. and Madara, J.L. (1996) Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils. Mol. Med. 2, 489-505
64. Colgan, S.P., Parkos, C.A., McGuirk, D., Brady, H.R., Papayianni, A.A., Frendl, G. and Madara, J.L. (1995) Receptors involved in carbohydrate binding modulate intestinal epithelial-neutrophil interactions. J. Biol. Chem. 270, 10531-10539
65. Diamond, M.S., Alon, R., Parkos, C.A., Quinn, M.T. and Springer, T.A. (1995) Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J. Cell Biol. 130, 1473-1482
66. Zen, K., Liu, Y., Cairo, D. and Parkos, C.A. (2002) CD11b/CD18-dependent interactions of neutrophils with intestinal epithelium are mediated by fucosylated proteoglycans. J. Immunol. 169, 5270-5278
67. Nusrat, A., Parkos, C.A., Liang, T.W., Carnes, D.K. and Madara, J.L. (1997) Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 113, 1489-1500
68. Edens, H.A., Levi, B.P., Jaye, D.I., Walsh, S., Reaves, T.A., Turner, J.R., Nusrat, A. and Parkos, C.A. (2002) Neutrophil transepithelial migration: evidence for sequential, contact-dependent signaling events and enhanced paracellular permeability independent of transjunctional migration. J. Immunol. 169, 476-486
69. Liu, Y., O'Connor, M.B., Mandell, K.J., Zen, K., Ullrich, A., Buhring, H.J. and Parkos, C.A. (2004) Peptide-mediated inhibition of neutrophil transmigration by blocking CD47 interactions with signal regulatory protein α. J. Immunol. 172, 2578-2585
70. Zen, K., Babbin, B.A., Liu, Y., Whelan, J.B., Nusrat, A. and Parkos, C.A. (2004) JAM-C is a component of desmosomes and a ligand for CD11b/CD18-mediated neutrophil transepithelial migration. Mol. Biol. Cell 15, 3926-3937
71. Zen, K. and Parkos, C.A. (2003) Leukocyte-epithelial interactions. Curr. Opin. Cell Biol. 15, 557-564
72. Hu, Y., Kiely, J.M., Szente, B.E., Rosenzweig, A. and Gimbrone, Jr, M.A. (2000) E-selectin-dependent signaling via the mitogen-activated protein kinase pathway in vascular endothelial cells. J. Immunol. 165, 2142-2148